Holloway joined the Northwestern faculty in July 2017 and began his term as provost a month later. Before moving to Northwestern, Holloway was the Edmund S. Morgan Professor of History, African American Studies, and American Studies at Yale University. He served as the Dean of Yale College from 2014 to 2017. Prior to the deanship he was the head of Calhoun (Hopper) College from 2005 to 2014.

He is a member of the Board of Directors for the Chicago Botanical Society, the National Humanities Alliance, the United States Air Force Air University, and the Society for United States Intellectual History.

Holloway has held fellowships from the W.E.B. Du Bois Research Institute at Harvard University, the Stanford Humanities Center, the Ford Foundation, and the Danforth Foundation. He was an Alphonse Fletcher Sr. Fellow in 2011-2012. Currently, he is a Distinguished Lecturer for the Organization of American Historians.